Nickel toxicity in embryos and larvae of the South American toad: Effects on cell differentiation, morphogenesis, and oxygen consumption

Abstract

Nickel, a widely distributed heavy metal in the biosphere, produces systemic, carcinogenic, and teratogenic effects. The objectives of the present study are to report the acute, short-term chronic, and chronic toxicity of Ni in Rhinella arenarum embryos as well as the stage-dependent susceptibility to this heavy metal, including oxygen consumption, teratogenesis, and adverse effects on cell differentiation processes. The stages evaluated were blastula (S.7), gastrula (S.11), tail bud (S.17), fin circulation (S.22), and complete operculum (S.25), in this last case by means of toxicity profile curves. Nickel increases its adverse effects gradually, with a maximum value after 96 h. The 50% lethal concentrations (LC50s) for 96, 168, and 240 h at S.25 were 1.14, 0.60, and 0.48 mg Ni²(+) /L, respectively; S.11 and S.22 were the least and most susceptible to Ni with, LC50s 96 h of 6.12 and 0.19 mg Ni²(+) /L, respectively. A reduction of approximately 25% in oxygen consumption anticipates lethal effects from S.17 onward. The main teratogenic effects were retarded growth and development, extremely severe axis incurvations, persistent yolk plug, asymmetry, microcephaly and mouth and gill agenesia, and limited neuromuscular activity. Ciliated cells were not functional. The possibility of associating the remarkable stage-dependent susceptibility to Ni with environmental changes during the evolutionary process is also considered.

Stage‐dependent susceptibility to copper in Rhinella arenarum embryos and larvae

“…Conversely, Cu toxicity in continuous treatment from complete operculum stage (S.25) onward did not significantly change along the exposure time (168 h), confirming previous results [24], in which Cu at this larval stage achieves its maximal toxicity within the initial 24 h of exposure. This pattern of fast maximal toxic effect found for Cu is similar to the results reported for Cd [19], whereas the toxicity of Ni significantly increased by expanding the evaluation period over 96 h, even if the metal exposure had been for only 24 h [20]. At advanced larval stages (S.28), the increase in the resistance to Cu was significant, up to 2.5 times higher than complete operculum stage (S.25); nevertheless, Cu toxicity increased toward metamorphosis.…”

“…As a whole, embryos at blastula (S.4) and gastrula (S.11) stages showed the highest resistance to Cu; the organogenic stages were the most susceptible, and during the last embryonic and larval stages the resistance to Cu increased gradually up to values obtained in the blastula and gastrula. This pattern within the embryonic stages has also been found with other metals, such as Pb [18] and Ni [20], and organic substances such as 2,4-dichlorophenoxyacetic acid Copper toxicity in amphibian early life stages Environ. Toxicol.…”

“…In comparison with other metals, the present results show that Cu was the most toxic for R. arenarum embryos followed by Cd [19], Ni [20], Al [31], and Pb [18]. Copper also caused relevant teratogenic effects in all the developmental stages evaluated.…”

“…For the stagedependent susceptibility studies, embryos and larvae at blastula (S.4), gastrula (S.11), neural plate (S.13), neural fold (S.14), tail bud (S.17), muscular response (S.18), gill circulation (S. 20), open mouth (S.21), opercular folds (S.23), right operculum closed (S.24), complete operculum (S.25), and hind limb bud (S.28) stages were 24-h pulse exposed to Cu.…”

“…Teratogenic effects of Cu, such as embryonic deformities, decreased growth rate, and delayed metamorphosis [16], as well as behavioral changes [17], have been reported. Toxicity studies performed by treating embryos and larvae during specific developmental stages allow the evaluation of stage-dependent susceptibility and the potential adverse effects related to specific cell differentiation and morphogenic processes, providing possible explanations based on well-known developmental features, toxicity mechanisms, and evolutionary perspective [12,[18][19][20]. The main aim of the present study was to evaluate the toxic effects of Cu on the South American toad Rhinella arenarum at different embryonic and larval stages, reporting lethality and malformations at optical and electronic microscopic levels.…”